Stereotactic radiosurgery for intracranial dural arteriovenous fistulas: a systematic review

Ching-Jen ChenDepartments of Neurological Surgery and

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Cheng-Chia LeeDepartments of Neurological Surgery and
Department of Neurosurgery, Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan; and

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Dale DingDepartments of Neurological Surgery and

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Robert M. StarkeDepartments of Neurological Surgery and

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Srinivas ChivukulaDepartment of Neurological Surgery, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania

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Chun-Po YenDepartments of Neurological Surgery and

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Shayan MoosaDepartments of Neurological Surgery and

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Zhiyuan XuDepartments of Neurological Surgery and

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David Hung-Chi PanDepartment of Neurosurgery, Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan; and

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Jason P. SheehanDepartments of Neurological Surgery and
Radiation Oncology, University of Virginia Health System, Charlottesville, Virginia;

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OBJECT

The goal of this study was to evaluate the obliteration rate of intracranial dural arteriovenous fistulas (DAVFs) in patients treated with stereotactic radiosurgery (SRS), and to compare obliteration rates between cavernous sinus (CS) and noncavernous sinus (NCS) DAVFs, and between DAVFs with and without cortical venous drainage (CVD).

METHODS

A systematic literature review was performed using PubMed. The CS DAVFs and the NCS DAVFs were categorized using the Barrow and Borden classification systems, respectively. The DAVFs were also categorized by location and by the presence of CVD. Statistical analyses of pooled data were conducted to assess complete obliteration rates in CS and NCS DAVFs, and in DAVFs with and without CVD.

RESULTS

Nineteen studies were included, comprising 729 patients harboring 743 DAVFs treated with SRS. The mean obliteration rate was 63% (95% CI 52.4%–73.6%). Complete obliteration for CS and NCS DAVFs was achieved in 73% and 58% of patients, respectively. No significant difference in obliteration rates between CS and NCS DAVFs was found (OR 1.72, 95% CI 0.66–4.46; p = 0.27). Complete obliteration in DAVFs with and without CVD was observed in 56% and 75% of patients, respectively. A significantly higher obliteration rate was observed in DAVFs without CVD compared with DAVFs with CVD (OR 2.37, 95% CI 1.07–5.28; p = 0.03).

CONCLUSIONS

Treatment with SRS offers favorable rates of DAVF obliteration with low complication rates. Patients harboring DAVFs that are refractory or not amenable to endovascular or surgical therapy may be safely and effectively treated using SRS.

ABBREVIATIONS

AVM = arteriovenous malformation; CS = cavernous sinus; CVD = cortical venous drainage; DAVF = dural arteriovenous fistula; GKS = Gamma Knife surgery; LINAC = linear accelerator; NCS = noncavernous sinus; SRS = stereotactic radiosurgery; TSS = transverse and sigmoid sinus.

OBJECT

The goal of this study was to evaluate the obliteration rate of intracranial dural arteriovenous fistulas (DAVFs) in patients treated with stereotactic radiosurgery (SRS), and to compare obliteration rates between cavernous sinus (CS) and noncavernous sinus (NCS) DAVFs, and between DAVFs with and without cortical venous drainage (CVD).

METHODS

A systematic literature review was performed using PubMed. The CS DAVFs and the NCS DAVFs were categorized using the Barrow and Borden classification systems, respectively. The DAVFs were also categorized by location and by the presence of CVD. Statistical analyses of pooled data were conducted to assess complete obliteration rates in CS and NCS DAVFs, and in DAVFs with and without CVD.

RESULTS

Nineteen studies were included, comprising 729 patients harboring 743 DAVFs treated with SRS. The mean obliteration rate was 63% (95% CI 52.4%–73.6%). Complete obliteration for CS and NCS DAVFs was achieved in 73% and 58% of patients, respectively. No significant difference in obliteration rates between CS and NCS DAVFs was found (OR 1.72, 95% CI 0.66–4.46; p = 0.27). Complete obliteration in DAVFs with and without CVD was observed in 56% and 75% of patients, respectively. A significantly higher obliteration rate was observed in DAVFs without CVD compared with DAVFs with CVD (OR 2.37, 95% CI 1.07–5.28; p = 0.03).

CONCLUSIONS

Treatment with SRS offers favorable rates of DAVF obliteration with low complication rates. Patients harboring DAVFs that are refractory or not amenable to endovascular or surgical therapy may be safely and effectively treated using SRS.

Current treatment strategies for intracranial dural arteriovenous fistulas (DAVFs) include microsurgical ligation, transarterial or transvenous embolization, stereotactic radiosurgery (SRS), and various combinations of these therapeutic options. Endovascular therapy, most commonly performed via transvenous routes, has become the preferred treatment approach for DAVFs.27,44,48 Due to the immediate obliteration that can be achieved with endovascular or surgical occlusion, SRS is typically reserved for lesions that cannot be obliterated with endovascular or surgical approaches, or for patients who pose a high surgical risk due to medical comorbidities. Therefore, published SRS series for DAVFs remain relatively few and comprise mostly retrospective, single-center studies.

In this systematic review, we evaluate the obliteration rate of DAVFs in patients treated with SRS. We also compare obliteration rates between cavernous sinus (CS) and noncavernous sinus (NCS) DAVFs, and between DAVFs with and without cortical venous drainage (CVD), by using available data in the literature.

Methods

Inclusion Criteria

In our attempt to balance between the largest possible patient population and a relatively homogeneous cohort, the following inclusion criteria for this systematic review were devised: 1) the study must contain at least 5 patients who had intracranial DAVFs treated with SRS without concurrent arteriovenous malformations (AVMs) or arterial aneurysms; 2) the study must have included post-SRS outcome data regarding DAVF obliteration rates; and 3) the language of the study must be English. Patients who underwent prior or combined therapies other than SRS for their DAVFs and/or had prior hemorrhages were not excluded.

Literature Search

A systematic literature review was performed on March 3, 2014, using PubMed with the following search term: “dural arteriovenous fistula OR arteriovenous fistula AND radiosurgery.” Following the search, the articles were then screened by title and abstract. The remaining articles underwent further detailed review for relevance and usable data matching the inclusion criteria. Articles with insufficient post-SRS data and overlapping published data from the same institution in a more recent study were excluded. However, those with partially overlapping but supplementary treatment outcomes data from the same institutions were not excluded from the review.

Literature Review and Data Extraction

No registered review protocol was used in this study. This review follows the guidelines set forth by the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) Statement. Available demographic, radiosurgical, and clinical and radiological outcomes data were extracted from studies that met the inclusion criteria. Demographic data included number of patients, sex, and age. Radiosurgical data included the type of SRS device used (i.e., Gamma Knife, linear accelerator, proton beam) and radiosurgical parameters (mean margin dose, isodose line, and treatment volume). Outcomes data reviewed for each study included duration of follow-ups, complete obliteration rates as determined using modalities specified by the respective studies, hemorrhages following SRS, SRS-related new or worsened neurological deficits, and SRS-related deaths.

The DAVFs were categorized by location (CS, transverse and sigmoid sinus [TSS], and other locations) whenever possible. The NCS DAVFs included those located at the TSS and other locations. The CS DAVFs were classified using the Barrow classification system, whereas NCS DAVFs were classified using the Borden classification system.4,5 For studies that used the Cognard classification system, patients were reclassified using the Borden classification system as follows: Cognard Types I and IIa were categorized as Borden Type I; Cognard Types IIb and IIa + b were categorized as Borden Type II; and Cognard Types III, IV, and V were categorized as Borden Type III.8 To assess the association between treatment outcomes and CVD, patients were also classified into groups of DAVFs without CVD (Borden Type I or Cognard Types I and IIa) and with CVD (Borden Types II and III or Cognard Types IIb, IIa + b, III, IV, and V). Table 1 outlines the Borden, Cognard, and Barrow classification systems.4,5,8

TABLE 1

Classification systems for DAVFs

Authors & CategoriesDescription
Cognard et al., 1995
 Type IDrainage into dural venous sinus w/normal antegrade flow
 Type IIaDrainage into dural venous sinus w/retrograde flow
 Type IIbDrainage into dural venous sinus w/normal antegrade flow & CVD
 Type IIa & IIbDrainage into dural venous sinus w/retrograde
 Type IIIDirect drainage into cortical vein w/o venous ectasia
 Type IVDirect drainage into cortical vein w/venous ectasia
 Type VDirect drainage into perimedullary veins
Borden et al., 1995
 Type IDrainage into dural venous sinus or meningeal vein
 Type IIDrainage into dural venous sinus & CVD
 Type IIIDirect drainage into cortical vein
Barrow et al., 1985
 Type ADirect high-flow shunts btwn ICA & CS
 Type BIndirect low-flow shunts btwn meningeal branches of ICA & CS
 Type CIndirect low-flow shunts btwn meningeal branches of ECA & CS
 Type DIndirect low-flow shunts btwn meningeal branches of both ICA & ECA & CS

ECA = external carotid artery; ICA = internal carotid artery.

Statistical Analysis

Descriptive statistics for this review were determined using SPSS version 20.0.0 (IBM Corp., 2011), whereas statistical analyses of pooled data comparing obliteration rates were performed using Review Manager version 5.2.8 (The Nordic Cochrane Centre; The Cochrane Collaboration, 2012). The DAVF obliteration rates following SRS were extracted for DAVFs with and without CVD, and for CS and NCS DAVFs. Studies with obliteration rates for DAVFs both with and without CVD were included in the meta-analysis comparing their respective obliteration rates. Similarly, studies with obliteration rates for both CS and NCS DAVFs were analyzed in the meta-analysis comparing their respective obliteration rates. Odds ratios for individual studies and the sum of the included studies were computed using the Mantel-Haenszel test.

Under the assumptions of possible clinical diversity and methodological differences among the included studies, the random effects model was implemented in the analyses for this review. Study heterogeneity was detected using the chi-square and I2 test statistics. However, the power of the chi-square test was limited by the inclusion of a small number of studies in the analyses; hence significant heterogeneity was considered to be present when both the chi-square value was within the 10% level of significance (p < 0.10) and the I2 value exceeded 50%. Potential contributions to variations across studies are discussed in the limitations section of this review. Unclear risks of bias were assumed for retrospective studies. All statistical tests were 2-sided, and p < 0.05 was considered statistically significant.

Results

Study Selection

The search yielded 1379 articles published between 1972 and 2014. The initial screening process led to the selection of 31 articles. Subsequently, 12 studies were excluded for reasons including insufficient post-SRS outcome data and overlapping published patient data from the same institution in another study. Finally, 19 series comprising 729 patients harboring 743 DAVFs who underwent SRS were identified.3,6,7,12,14,16,19,20,22,23,31–34,37,39,41,42,51 Figure 1 demonstrates an outline of the systematic review process. Four studies with partially overlapping but supplementary treatment outcomes data from two institutions were included in the systematic review. However, no two studies from the same institution were included in the same part of the analyses. All studies included were retrospective in design, comprising mostly small cohorts. Unclear risks of bias were assigned to all studies.

FIG. 1
FIG. 1

Flowchart outlining the systematic review process. The initial PubMed search yielded 1379 articles, and the subsequent screening process led to the selection of 31 articles to undergo further detailed review for relevance and usable data matching the inclusion criteria. Twelve studies were excluded for reasons including insufficient post-SRS outcome data and overlapping published patient data from the same institution in another study. Finally, 19 series comprising 729 patients harboring 743 DAVFs who underwent SRS were identified and included in the review.

Overall Demographic Data, DAVF and Treatment Characteristics, and Outcomes

There was a slight female predominance among the 19 included studies, with 312 of the 580 patients (53.8%) with available demographic information identified as female. The mean patient age for the 19 studies ranged between 50 years and 69 years. The SRS modalities used were Gamma Knife surgery (GKS) and linear accelerator (LINAC)–based radiosurgery in 15 and 3 studies, respectively; in 1 study the specific SRS modality used was not documented. Prior endovascular embolizations and microsurgeries were performed in 199 of 701 (28.4%) and 34 of 726 (4.7%) of DAVFs, respectively. The mean follow-up period after SRS ranged from 12 months to 50 months (overall mean 28.9 months).

Combining the results of the included studies, in 438 of 642 DAVFs (68.2%) with follow-up data, complete obliteration was achieved following SRS. The mean obliteration rate between individual studies was 63% (95% CI 52.4%–73.6%). Angiography was performed in 292 patients, and complete obliteration was observed in 255 (87.3%). Post-SRS hemorrhage, new or worsened neurological deficit, and death occurred in 9 of 730 DAVFs (1.2%), 9 of 715 patients (1.3%), and 2 of 715 patients (0.3%), respectively. A summary of included SRS series for DAVFs along with the respective radiosurgical parameters is found in Table 2.

TABLE 2

Summary of the 19 SRS series for DAVFs included in this systematic review

Authors & YearNo. of PtsNo. Female PtsMean Age (yrs)No. DAVFsMean Radio FU (mos)Previous Embo, n/NPrevious Microsurgery, n/NSRS ModalityMean Margin Dose (Gy)Isodose Line (%)Tx Vol (cm3)Complete Oblit, n/NComplete Oblit on Angio, n/NNo. w/ Post-SRS HemNo. w/ Other Neuro DefsNo. Dead
Pan et al., 2013*32118057.832121 for CS, 28 for NCS41/32113/321GKS17.268.5 for CS, 57.7 for NCS4.7 for CS, 16.9 for NCS173/264NA201
Piippo et al., 201316NANA17NA13/170/17LINAC18NANA9/17NA000
Söderman et al., 2013*65NANA67NA10/673/67GKS20–2540–60NA37/6337/63220
Gross et al., 2012148356.89354/90/9LINAC17.7NA18/9NA000
Oh et al., 201243NANA43NA30/430/43GKS19NA6.932/4332/43110
Hanakita et al., 201222857222710/222/22GKS21NA1.512/229/18000
Yang et al., 2010401869444519/440/44GKS2050 in 42, 60 in 2232/4421/44101
Cifarelli et al., 2010551850553636/5511/55GKS21NANA30/4630/46310
Kida, 200913454.313247/130/13GKS18.9NANA5/13NA000
Söderman et al., 2006*49NANA52NA7/523/52GKS22NANA28/4128/41210
Koebbe et al., 200518965234613/230/23GKS20NA2.1615/188/8010
Pan et al., 2002*209532019NANAGKS16.5–1950–701.7–40.711/199/9000
O'Leary et al., 20021610561724NANAGKS25, except 1 w/20.8350NA10/1310/13010
Chung et al., 20028656.38173/81/8GKS2070NA1/8NA010
Friedman et al., 200123185723212/230/23GKS18NA9.67/177/17000
Pollock et al., 199920176720122/200/20GKS20502.813/1513/15010
Link et al., 199629176129NA2/291/29GKS19.250 603.313/1813/18000
Lewis et al., 199474617247/70/7LINAC15.6NANA3/73/7010
Barcia-Salorio et al., 199425NANA2550NA3/25NA30 40, except 1 w/ 20NANA21/25NA000
Total§729312/580 (53.8%)743199/701 (28.4%)34/726 (4.7%)438/642 (68.2%)255/292 (87.3%)9/730 (1.2%)9/715 (1.3%)**2/715 (0.3%)**

Angio = angiography; embo = embolization; FU = follow-up; hem = hemorrhage; NA = not available; neuro defs = neurological deficits; oblit = obliteration; pts = patients; radio = radiological; Tx = treatment.

Studies with partially overlapping but complementary treatment outcomes data from the same institution.

Distinction between clinical and radiological follow-up unclear.

Studies with patients treated with combined endovascular embolization and SRS.

Excludes earlier studies with partially overlapping but complementary treatment outcomes data from the same institutions.

Based on the number of DAVFs in patients with follow-up.

Based on the number of patients with follow-up.

Outcomes for CS DAVFs Versus NCS DAVFs

Of the 700 DAVFs categorized by location, 323 (46.1%) were located in the region of the CS and 377 (53.9%) were located in NCS regions. Complete obliteration was achieved in 172 of 236 CS DAVFs (72.9%) and in 143 of 247 NCS DAVFs (57.9%). Post-SRS hemorrhages were observed in 0 of 295 patients with CS DAVF and in 3 of 237 patients with NCS DAVF (1.3%). The NCS DAVFs comprised 192 TSS DAVFs (50.9%) and 185 DAVFs at other locations (49.1%). Complete obliteration was observed in 52 of 87 TSS DAVFs (59.8%) and in 38 of 71 DAVFs at other NCS, non-TSS locations (53.5%). Post-SRS hemorrhages were reported in 2 of 142 patients with TSS DAVFs (1.4%) and in 1 of 95 patients with NCS, non-TSS DAVFs (1.1%). A summary of CS and NCS DAVF treatment outcomes following SRS is found in Table 3. Despite the difference in complete obliteration rates between CS and NCS DAVFs, analysis of pooled data based on the random effects model from 5 studies with DAVF obliteration data for both CS and NCS DAVFs demonstrated no significant difference in their complete obliteration rates (OR 1.72, 95% CI 0.66–4.46; p = 0.27). No significant heterogeneity among the included studies was found in this analysis (χ2 = 5.71; p = 0.22; I2 = 30%). Results of the analysis are summarized in Fig. 2.

TABLE 3

Summary of DAVF treatment outcomes following SRS in lesions characterized by location and type

CharacteristicNo. DAVFs (%)Complete Oblit, n/N (%)Post-SRS Hem, n/N (%)
DAVF location
 CS323 (46.1)172/236 (72.9)0/295 (0.0)
 NCS377 (53.9)143/247 (57.9)3/237 (1.3)
  TSS192 (50.9)52/87 (59.8)2/142 (1.4)
  Others185 (49.1)38/71 (53.5)1/95 (1.1)
CS DAVFs
 Barrow Type A3 (1.2)1/3 (33.3)0/3 (0.0)
 Barrow Type B31 (12.4)11/11 (100.0)0/31 (0.0)
 Barrow Type C19 (7.6)3/4 (75.0)0/19 (0.0)
 Barrow Type D198 (78.9)6/7 (85.7)0/198 (0.0)
NCS DAVFs
 Borden Type I105 (47.7)52/79 (65.8)0/85 (0.0)
 Borden Type II60 (27.3)15/35 (42.9)1/38 (2.6)
 Borden Type III55 (25.0)12/24 (50.0)1/27 (3.7)
CVD
 DAVFs w/o CVD157 (48.8)76/102 (74.5)0/131 (0.0)
 DAVFs w/ CVD165 (51.2)69/123 (56.1)6/144 (4.2)
FIG. 2
FIG. 2

Forest plot of the ORs of obliteration rates for CS and NCS DAVFs treated with SRS. The estimated OR and 95% CI for each included study are represented by the center of the squares and the horizontal line, respectively. The summary OR and 95% CI are shown in bold, and are represented by the diamond. Tests of heterogeneity and overall effect are given below the summary statistics. M-H = Mantel-Haenszel. Figure is available in color online only.

Outcomes for DAVFs With CVD Versus DAVFs Without CVD

In studies that reported CS DAVFs using the Barrow classification system, 3 (1.2%), 31 (12.4%), 19 (7.6%), and 198 (78.9%) were categorized as Barrow Types A, B, C, and D DAVFs, respectively. Complete obliteration was observed in 1 of 3 Type A (33.3%), in 11 of 11 Type B (100%), in 3 of 4 Type C (75%), and 6 of 7 Type D (85.7%) CS DAVFs. No post-SRS hemorrhages were reported in any of the CS DAVFs. Among studies that reported NCS DAVFs using the Borden classification system, 105 (47.7%), 60 (27.3%), and 55 (25.0%) were categorized as Borden Types I, II, and III, respectively. Complete obliteration was observed in 52 of 79 Borden Type I (65.8%), 15 of 35 Type II (42.9%), and 12 of 24 Type III (50.0%) NCS DAVFs. Post-SRS hemorrhages were reported in 0 of 85 patients with Borden Type I, in 1 of 38 patients with Type II (2.6%), and in 1 of 27 patients with Type III (3.7%) DAVFs. A summary of SRS outcomes for CS and NCS DAVFs categorized using the Barrow and Borden classification systems is found in Table 3.

Of the 322 DAVFs with known venous drainage patterns, 165 (51.2%) had associated CVD and 157 (48.8%) did not have CVD. Complete obliteration was observed in 69 of 123 DAVFs (56.1%) with CVD and in 76 of 102 DAVFs (74.5%) without CVD. Post-SRS hemorrhage was reported in 6 of 144 DAVFs with CVD (4.2%) and in 0 of 131 DAVFs without CVD (0.0%). A summary of SRS outcomes for DAVFs with and without CVD is found in Table 3. Analysis of pooled data based on the random effects model demonstrated that DAVFs without CVD were associated with a significantly higher rate of complete obliteration following SRS compared with DAVFs with CVD among 9 studies with obliteration data for DAVFs both with and without CVD (OR 2.37, 95% CI 1.07–5.28; p = 0.03). No significant heterogeneity among the included studies was found in this analysis (χ2 = 8.93; p = 0.35; I2 = 10%). Results of the analysis are summarized in Fig. 3.

FIG. 3.
FIG. 3.

Forest plot of the ORs of obliteration rates for DAVFs with and without CVD treated with SRS. The estimated OR and 95% CI of each included study are represented by the center of the squares and the horizontal line, respectively. The summary OR and 95% CI are shown in bold, and are represented by the diamond. Tests of heterogeneity and overall effect are given below the summary statistics. Figure is available in color online only.

Only a few studies investigated the potential factors associated with complete obliteration of DAVFs following SRS. Conflicting factors were found between these studies. Factors found by the included studies to be significantly associated with obliteration are as follows: CS DAVFs, Borden Type I DAVFs, DAVFs without CVD, hemorrhage at presentation, target volume < 1.5 ml, and Cognard Types III or IV DAVFs.7,16,51 Factors found to be nonsignificant are as follows: patient age and sex, prior treatments, DAVF location and size, DAVFs with multiple arteriovenous connections versus DAVFs with single arteriovenous connections, and minimal radiation dose delivered to DAVFs.7,16,42 Table 4 outlines these factors investigated by studies included in this systematic review.

TABLE 4

Factors associated with DAVF obliteration via SRS among included studies

Authors & YearAssociated w/ DAVF OblitNot Associated w/ DAVF Oblit
Yang et al., 2013CS DAVFs
Cifarelli et al., 2010Borden Type I DAVFsSex
No CVDPrior endovascular therapy for DAVF
Prior craniotomy for DAVF
Location of DAVF
Size of DAVF
Multi-hole vs single-hole DAVF
Hanakita et al., 2012No CVDAge
Hem at presentationSex
Target vol <1.5 mlLocation of DAVF
Cognard Types III or IV DAVFPrior therapy
Söderman et al., 2006Minimal radiation dose to
DAVF

Discussion

Stereotactic radiosurgery was initially used in the treatment of AVMs in 1970 and was subsequently used to treat DAVFs in the late 1970s. Barcia-Salorio and colleagues first reported the use of SRS for treating DAVFs in 1982, followed by an SRS case series for DAVFs composed of 25 cases of CS DAVFs in 1994.2,3 Since then, a number of other studies have investigated the use of SRS for treating DAVFs in other locations, with variable rates of success. This systematic review of the literature, comprising 19 studies, found a reasonable rate of complete DAVF obliteration (63%), with relatively low complication rates. Although the complete obliteration rate determined using angiography is higher (87.3%), this may be biased because invasive modalities such as angiography are often performed to confirm complete obliteration following obliteration observed using noninvasive imaging modalities. The associated rates of post-SRS hemorrhage, neurological deficit, and mortality were 1.2%, 1.3%, and 0.3%, respectively. However, variations in obliteration and complication rates, such as risks of hemorrhage, may be dependent on factors such as the location and angioarchitecture of DAVFs. Therefore, we also categorized SRS treatment outcomes for DAVFs by location and venous drainage pattern.

Comparison of CS DAVFs and NCS DAVFs

Cavernous sinus DAVFs represent a subset of lesions that are distinct from NCS DAVFs. In contrast to other intracranial dural venous sinuses, the CS is located extradurally, not between the periosteal and meningeal layers.17,18 Due to its many routes of venous drainage, the presenting symptoms and signs of a CS DAVF are often benign.46 These symptoms include blurred vision, bruit, diplopia, exophthalmos, chemosis, and glaucoma. Given the benign features of low-flow CS DAVFs and possibility of spontaneous occlusion, some authors have advocated conservative treatments, including cervical carotid artery and jugular vein compressions, as first-line therapies for these lesions.15,40 However, some cases present with intractable intraocular hypertension or reduced ocular perfusion pressure, thereby warranting more rapid interventions to prevent progressive vision loss.36,40,49

Due to their unique anatomy and symptomatology, CS DAVFs are often categorized using the Barrow classification system.4 Type A fistulas represent direct high-flow shunts between the internal carotid artery and the CS, comprising mostly traumatic fistulas formed as a result of a tear in the cavernous segment of the internal carotid artery. These fistulas do not typically resolve spontaneously, and therefore require rapid intervention for cases of progressive visual loss. Barrow Type A CS DAVFs are often adequately treated via endovascular approaches, which provide immediate results. Thus, the number of Type A CS DAVFs treated using SRS is low (1.2% of reported CS DAVFs).10,25,26,28 Because complete obliteration of DAVFs following SRS is delayed, with a typical latency period of 1–3 years, SRS may represent a more suitable treatment modality for indirect, low-flow CS DAVFs classified as Barrow Types B, C, and D. In the largest SRS series for CS DAVFs to date, Pan et al. observed a complete obliteration rate of 70% with no reported cases of post-SRS hemorrhage or neurological morbidity in 156 indirect low-flow CS DAVFs.34 Based on the compiled data from studies included in this review, a complete obliteration rate of 73% was achieved in CS DAVFs treated with SRS. Therefore, the decision between conservative management and intervention should be individualized for each patient; consideration should be given to the severity of symptoms, DAVF angioarchitecture, and the efficacy and safety of treatments.

Noncavernous sinus DAVFs also comprise a heterogeneous cohort of lesions with variable presenting symptoms. Patients with DAVFs involving the TSS often present with pulsatile tinnitus and bruit, and those with superior sagittal sinus DAVFs can suffer from progressive dementia.21 Intracranial hemorrhage, the most devastating presentation of DAVFs, is more commonly seen in DAVFs involving the tentorium or anterior fossa.1,21 To better characterize DAVF hemorrhagic risk, the Borden and Cognard classification systems are used.5,8,9 Borden Types II and III and Cognard Types IIb–V DAVFs confer significantly higher risks of hemorrhage than Borden Type I and Cognard Types I and IIa DAVFs. Thus, these highrisk DAVFs usually warrant more immediate treatments in which modalities such as endovascular embolization and microsurgical ligation are used.9 As reflected in our results, fewer Borden Types II and III DAVFs were treated using SRS than Type I lesions. In the largest series of NCS DAVFs treated using SRS, Pan et al. observed a similar trend.34 Compared with the post-SRS obliteration rate for CS DAVFs (73%), the rate for NCS DAVFs appears to be lower (60%). However, this difference was not statistically significant in the pooled data analysis (p = 0.27). Post-SRS hemorrhage was observed more frequently in NCS DAVFs (1.3%) than in CS DAVFs (0%). Further categorization of NCS DAVFs demonstrated comparable obliteration rates for TSS DAVFs (60%) and DAVFs in other non-TSS locations (54%). Therefore, the efficacy of SRS does not seem to be restricted by DAVF location. More emphasis should be placed on understanding the angioarchitecture of DAVFs when selecting patients for SRS treatment.

Comparison of DAVFs With CVD and DAVFs Without CVD

It is well recognized that DAVFs with CVD have a significantly greater risk of hemorrhage compared with those without CVD. Söderman et al. reported a 1.5% annual risk of hemorrhage in 53 patients with unruptured DAVFs with CVD.43 In the same study, this risk increased to 7.4% per year for those with ruptured DAVFs. Strom et al. reported a similar annual hemorrhage rate of 1.4% in 17 patients harboring DAVFs with CVD without prior hemorrhage.45 The risk increased to 7.6% in those with DAVFs with CVD who presented with hemorrhage or nonhemorrhagic neurological deficit. Detailed analyses by Gross and Du of published studies found 6% and 10% annual hemorrhage rates for Borden Types II and III DAVFs, respectively, in contrast to an annual hemorrhage rate of 0% for Borden Type I DAVFs.13 Although an annual hemorrhage rate of 3% for unruptured DAVFs with CVD was found in their study, the rate increased to 46% per year for ruptured DAVFs with CVD. The recurrence of bleeding can occur within the first few weeks following the initial hemorrhage. Duffau et al. observed a rebleeding rate of 35% within the first 2 weeks after the initial hemorrhage.11 Significant mortality rates of up to 10.4% annually have been associated with the persistence of CVD.47

Given the high morbidity and mortality rates observed in untreated or partially treated DAVFs with CVD, urgent treatment using modalities that offer immediate obliteration should be recommended for these lesions. Due to the risk of hemorrhage during the latency period between treatment and obliteration, SRS should not be recommended as the sole and/or first-line treatment for DAVFs with CVD. In this systematic review, we observed a higher risk of post-SRS hemorrhage for DAVFs with CVD compared with those without CVD (4.2% vs 0%). In addition, we found a significantly lower obliteration rate for SRStreated DAVFs with CVD compared with those without CVD (p = 0 .03). Therefore, patients harboring DAVFs with CVD should undergo endovascular embolization, microsurgical resection, or a combination of the two as initial therapy to rapidly reduce or eliminate the risk of hemorrhage. Stereotactic radiosurgery can be offered as an adjuvant or salvage therapy in cases refractory to embolization or surgery.29 For patients harboring DAVFs without CVD, the decision to treat should be based on the severity of symptoms. Close observation should be recommended to patients with nondisabling symptoms, whereas SRS and/or endovascular embolization should be reserved for those with intractable symptoms.

In patients selected to undergo endovascular embolization, SRS may represent an effective complementary therapy.7,12,22,23,35,39,51 Although endovascular embolization may provide immediate symptomatic relief and reduction of hemorrhage risk, the treatment may not afford longterm cure in cases of subtotal obliteration or delayed recanalization.24 Therefore, SRS serves as a complementary treatment by potentially increasing the likelihood of permanent DAVF occlusion.24,51 However, the timing of embolization and SRS remains controversial. Some authors argue that embolization prior to SRS can reduce target volume and blood flow, thus facilitating obliteration by SRS. In contrast, others contend that the target margin may be obscured when embolization is performed prior to SRS, resulting in inadequate target delineation and ineffective treatment.

Study Limitations

This systematic review is limited by the pooled data available from largely retrospective, single-center studies, with all of the limitations and weaknesses inherent to retrospective designs. In an attempt to reduce the nuances separating detailed classification systems, best efforts were made to classify DAVFs into broader categories. Not all studies were included in this systematic analysis; insufficient DAVF obliteration outcomes data led to the exclusion of certain studies from analyses. Insufficient outcomes data from some studies also limit certain comparative statistical analyses. Despite no significant findings in the tests of heterogeneity, the variability in the methods of clinical evaluation and determination of complete DAVF obliteration among studies remains difficult to overcome.

Verification of complete obliteration varied depending on the study institution; MRI or MR angiography, digital subtraction angiography, or a combination of these imaging modalities may have been used in different studies. Ideally, obliteration would be confirmed with cerebral angiography. However, when this is not advisable or the patient refuses, MRI and MR angiography or CT and CT angiography have been shown to be reasonable surrogates for cerebral AVMs, and this approach has been extended to DAVFs in contemporary practice.30,38 In addition, baseline characteristics of patients may vary significantly. Stereotactic radiosurgery was not the primary or sole treatment for all patients in this review; some patients underwent prior microsurgical ligation and/or embolization of their DAVFs. Patients in this review may also have been selected for SRS due to poor candidacy for microsurgery and/or embolization, or due to patient preference. However, data from these studies were insufficient to make such a distinction. Also, we did not differentiate results based on the type of SRS device used (e.g., LINAC, GKS, and so on) and cannot be certain if the results here are generalizable to all SRS platforms. Thus, results of this review should be interpreted with caution, and they may not be generalizable to all patients.

Conclusions

Stereotactic radiosurgery affords favorable rates of complete DAVF obliteration with acceptably low complication rates. Obliteration rates do not differ significantly between CS DAVFs and NCS DAVFs. However, DAVFs without CVD are associated with significantly higher obliteration rates than DAVFs with CVD. Therefore, careful patient selection for SRS based on DAVF angioarchitecture and hemorrhage risk is recommended. For DAVFs with CVD, SRS should be used as an adjuvant or salvage therapy. However, for DAVFs without CVD, SRS may be considered as a first-line therapy for patients who are unable or unwilling to undergo endovascular or surgical intervention, or it may be used in combination with embolization.

Author Contributions

Conception and design: Chen, Lee. Acquisition of data: Chen. Analysis and interpretation of data: Chen, Lee. Drafting the article: Chen, Lee, Ding. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Sheehan. Statistical analysis: Chen.

References

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    • Export Citation
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    • Search Google Scholar
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    • Search Google Scholar
    • Export Citation
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    Yang HC, , Kano H, , Kondziolka D, , Niranjan A, , Flickinger JC, & Horowitz MB, et al.: Stereotactic radiosurgery with or without embolization for intracranial dural arteriovenous fistulas. Neurosurgery 67:12761285, 2010

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  • Collapse
  • Expand
  • View in gallery

    Flowchart outlining the systematic review process. The initial PubMed search yielded 1379 articles, and the subsequent screening process led to the selection of 31 articles to undergo further detailed review for relevance and usable data matching the inclusion criteria. Twelve studies were excluded for reasons including insufficient post-SRS outcome data and overlapping published patient data from the same institution in another study. Finally, 19 series comprising 729 patients harboring 743 DAVFs who underwent SRS were identified and included in the review.

  • View in gallery

    Forest plot of the ORs of obliteration rates for CS and NCS DAVFs treated with SRS. The estimated OR and 95% CI for each included study are represented by the center of the squares and the horizontal line, respectively. The summary OR and 95% CI are shown in bold, and are represented by the diamond. Tests of heterogeneity and overall effect are given below the summary statistics. M-H = Mantel-Haenszel. Figure is available in color online only.

  • View in gallery

    Forest plot of the ORs of obliteration rates for DAVFs with and without CVD treated with SRS. The estimated OR and 95% CI of each included study are represented by the center of the squares and the horizontal line, respectively. The summary OR and 95% CI are shown in bold, and are represented by the diamond. Tests of heterogeneity and overall effect are given below the summary statistics. Figure is available in color online only.

  • 1

    Awad IA, , Little JR, , Akarawi WP, & Ahl J: Intracranial dural arteriovenous malformations: factors predisposing to an aggressive neurological course. J Neurosurg 72:839850, 1990

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2

    Barcia-Salorio JL, , Herandez G, , Broseta J, , Gonzalez-Darder J, & Ciudad J: Radiosurgical treatment of carotid-cavernous fistula. Appl Neurophysiol 45:520522, 1982

    • Search Google Scholar
    • Export Citation
  • 3

    Barcia-Salorio JL, , Soler F, , Barcia JA, & Hernández G: Stereotactic radiosurgery for the treatment of low-flow carotidcavernous fistulae: results in a series of 25 cases. Stereotact Funct Neurosurg 63:266270, 1994

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4

    Barrow DL, , Spector RH, , Braun IF, , Landman JA, , Tindall SC, & Tindall GT: Classification and treatment of spontaneous carotid-cavernous sinus fistulas. J Neurosurg 62:248256, 1985

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5

    Borden JA, , Wu JK, & Shucart WA: A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg 82:166179, 1995. (Erratum in J Neurosurg 82: 705–706, 1995)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6

    Chung SJ, , Kim JS, , Kim JC, , Lee SK, , Kwon SU, & Lee MC, et al.: Intracranial dural arteriovenous fistulas: analysis of 60 patients. Cerebrovasc Dis 13:7988, 2002

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7

    Cifarelli CP, , Kaptain G, , Yen CP, , Schlesinger D, & Sheehan JP: Gamma knife radiosurgery for dural arteriovenous fistulas. Neurosurgery 67:12301235, 2010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8

    Cognard C, , Gobin YP, , Pierot L, , Bailly AL, , Houdart E, & Casasco A, et al.: Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 194:671680, 1995

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9

    Davies MA, , TerBrugge K, , Willinsky R, , Coyne T, , Saleh J, & Wallace MC: The validity of classification for the clinical presentation of intracranial dural arteriovenous fistulas. J Neurosurg 85:830837, 1996

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Debrun G, , Lacour P, , Vinuela F, , Fox A, , Drake CG, & Caron JP: Treatment of 54 traumatic carotid-cavernous fistulas. J Neurosurg 55:678692, 1981

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    Duffau H, , Lopes M, , Janosevic V, , Sichez JP, , Faillot T, & Capelle L, et al.: Early rebleeding from intracranial dural arteriovenous fistulas: report of 20 cases and review of the literature. J Neurosurg 90:7884, 1999

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12

    Friedman JA, , Pollock BE, , Nichols DA, , Gorman DA, , Foote RL, & Stafford SL: Results of combined stereotactic radiosurgery and transarterial embolization for dural arteriovenous fistulas of the transverse and sigmoid sinuses. J Neurosurg 94:886891, 2001

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Gross BA, & Du R: The natural history of cerebral dural arteriovenous fistulae. Neurosurgery 71:594603, 2012

  • 14

    Gross BA, , Ropper AE, , Popp AJ, & Du R: Stereotactic radiosurgery for cerebral dural arteriovenous fistulas. Neurosurg Focus 32:5 E18, 2012

  • 15

    Halbach VV, , Higashida RT, , Hieshima GB, , Reicher M, , Norman D, & Newton TH: Dural fistulas involving the cavernous sinus: results of treatment in 30 patients. Radiology 163:437442, 1987

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16

    Hanakita S, , Koga T, , Shin M, , Shojima M, , Igaki H, & Saito N: Role of Gamma Knife surgery in the treatment of intracranial dural arteriovenous fistulas. J Neurosurg 117 Suppl:158163, 2012

    • Search Google Scholar
    • Export Citation
  • 17

    Kehrli P, , Ali M, , Reis M Jr, , Maillot C, , Dietemann JL, & Dujovny M, et al.: Anatomy and embryology of the lateral sellar compartment (cavernous sinus) medial wall. Neurol Res 20:585592, 1998

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18

    Kerber CW, & Newton TH: The macro and microvasculature of the dura mater. Neuroradiology 6:175179, 1973

  • 19

    Kida Y: Radiosurgery for dural arteriovenous fistula. Prog Neurol Surg 22:3844, 2009

  • 20

    Koebbe CJ, , Singhal D, , Sheehan J, , Flickinger JC, , Horowitz M, & Kondziolka D, et al.: Radiosurgery for dural arteriovenous fistulas. Surg Neurol 64:392399, 2005

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21

    Lasjaunias P, , Chiu M, , ter Brugge K, , Tolia A, , Hurth M, & Bernstein M: Neurological manifestations of intracranial dural arteriovenous malformations. J Neurosurg 64:724730, 1986

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Lewis AI, , Tomsick TA, & Tew JM Jr: Management of tentorial dural arteriovenous malformations: transarterial embolization combined with stereotactic radiation or surgery. J Neurosurg 81:851859, 1994

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    Link MJ, , Coffey RJ, , Nichols DA, & Gorman DA: The role of radiosurgery and particulate embolization in the treatment of dural arteriovenous fistulas. J Neurosurg 84:804809, 1996

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    Loumiotis I, , Lanzino G, , Daniels D, , Sheehan J, & Link M: Radiosurgery for intracranial dural arteriovenous fistulas (DAVFs): a review. Neurosurg Rev 34:305315, 2011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25

    Luo CB, , Teng MM, , Chang FC, & Chang CY: Endovascular treatment of intracranial high-flow arteriovenous fistulas by Guglielmi detachable coils. J Chin Med Assoc 69:8085, 2006

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26

    Luo CB, , Teng MM, , Chang FC, , Lin CJ, , Guo WY, & Chang CY: Transarterial detachable coil embolization of direct carotidcavernous fistula: immediate and long-term outcomes. J Chin Med Assoc 76:3136, 2013

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27

    Macdonald JH, , Millar JS, & Barker CS: Endovascular treatment of cranial dural arteriovenous fistulae: a single-centre, 14-year experience and the impact of Onyx on local practise. Neuroradiology 52:387395, 2010

    • Crossref
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    • Export Citation
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